Eight Little Piggies (38 page)

This complexity becomes important in Ryan’s argument for an interesting reason based on the physiology of amphibian hearing. Uniquely among terrestrial vertebrates, amphibians possess two inner-ear organs that pick up airborne vibrations—the amphibian papilla and the basilar papilla. The amphibian papilla is most sensitive to frequencies below 1200 Hz, while the basilar papilla responds best to higher frequencies above 1500 Hz.

Direct study of the inner ear in
Physalaemus pustulosus
shows that the most sensitive fibers of the amphibian papilla are tuned to about 500 Hz, while all fibers in the basilar papilla are most sensitive to about 2100 Hz. These facts suggest an obvious hypothesis for evolution of the complex call in
P. pustulosus
, particularly for the addition of chucks to the presumed ancestral call of whine alone—namely, that the whine only stimulates the amphibian papilla, while addition of the chuck takes advantage of a latent capacity already present but unutilized in ancestral calls: the acoustical properties of a basilar papilla tuned to higher frequencies concentrated in the chuck. The basilar papilla provides the preexisting sensory bias (sensitivity to higher frequencies), and the chuck finally contacts this everpresent, but initially unexploited, capacity.

Since the calls elicit female attention (with approach and eventual mating), Ryan and colleagues performed an interesting and successful experiment. They synthesized a variety of calls and broadcast two different versions from opposite ends of an indoor arena measuring 3 square meters. They put a female in the center of the arena and covered her with an opaque cone. They gave her five minutes to acclimate as they played the calls. A remote device then lifted the cone, and the female was free to approach a speaker. If she consistently preferred one to another, then the relative evolutionary value of whines and chucks might be assessed.

Females consistently favored the complex call of whine plus chuck over the whine alone. This preference is not a simple result of adding more total energy by including the chucks, but seems to be set by distinctive characters of the chuck. If females are given a choice between whine plus chuck and an enhanced whine alone (with 50 percent more total energy than whine plus chuck), they still prefer the complex call of whine plus chuck, despite its lower energy. Finally, Ryan and colleagues determined that females respond equally well to both the low and the high harmonics of the chuck. In other words, they are equally positive towards components of the chuck that stimulate either the amphibian or the basilar papilla.

So far so good. The added chuck does elicit female preference, and the component of the chuck that stimulates the previously unexploited basilar papilla also appeals to females. But to argue for the preexisting sensory bias model, we need to know that ancestral species (or relatives maintaining the ancestral state) are also inclined to react favorably to the chuck, even though their distinctive call contains no such component—just as Basolo showed that females in unarmored species prefer males with surgically implanted swords. Ryan was able to supply this final piece of evidence by measuring the tuning of basilar papillas in seven individuals of the closely related species,
Physalaemus coloradorum
. Ryan writes: “This species does not produce chucks, and the ability to produce chucks was derived in
P. pustulosus
after these species diverged.” Ryan found no statistically significant difference between the most sensitive frequencies for
P. pustulosus
(2130 Hz) and for the chuckless
P. coloradorum
(2230 Hz). The basilar papilla of
P. coloradorum
is therefore tuned to high frequencies not found in their actual call. A preexisting sensory bias for potentially advantageous evolutionary change can therefore be specified—a pathway actually followed by
P. pustulosus
.

These conclusions about preexisting sensory bias, while satisfying, also present another paradox. How can something so specific as the preference for an extension to a tail or a funny sound be encoded by accident into ancestral behaviors? Can we seriously believe that an animal might be adapted to favor swords never seen or chucks never heard?

The probable resolution of this paradox (another logical frustration in the terms of my introduction) may be illustrated by a famous experiment on quail, done ten years ago by the British ethologist Patrick Bateson (see bibliography). Avoidance of incest is very common in vertebrates with complex behaviors and high cognitive capacity. The evolutionary rationale is easy to express: Mating with closest kin produces a high frequency of genetically compromised offspring with disadvantageous traits in double recessive doses (a phenomenon called
inbreeding depression
). But quail don’t know Mendelian genetics (and neither did people before this century). So what can be leading animals to this evolutionarily advantageous behavior?

Bateson built an ingenious device that exposed individual quail to five birds of the opposite sex, but of different degrees of relationship: a sibling nestmate, a sibling never seen before, a first cousin, a third cousin, and an unrelated bird. Both males and females generally preferred first cousins over all alternatives.

One popular hypothesis (applicable to humans in some interpretations) holds that we avoid closest kin by a simple learning rule that derails later sexual feelings towards individuals reared with us from our earliest days (as one wag said, if we share potties early, we don’t party later—and remember, where I live in Boston, the two words are pronounced nearly alike). On this argument, since rearingmates are usually sibs, the simple learning rule turns the proper evolutionary trick. But this explanation will not suffice for Bateson’s data, for quail prefer first cousins over true siblings never seen before.

Bateson therefore concludes, from this and other arguments, that quail may be following a highly abstract aesthetic rule—prefer intermediary degrees of familiarity: not so close as to be cloying, not so distant as to be overly strange. If he is right, an elegant solution to the problem of avoiding incest suggests itself. Quail are not Mendelian calculators. They are, rather, following a deeper, and more abstract, rule of aesthetic preference that may be common to a wide range of animals and neurologies. Maximal attraction to intermediate familiarity will automatically exclude disadvantageous closest kin as potential mates. Natural selection need not work for the specific goal of avoiding incest. By good fortune, a deeper cognitive principle engenders this result as a consequence. (Of course, one might turn the argument around and claim that the aesthetic principle arose because incest avoidance is so important, and animals could only achieve this result by such an indirect route. But I prefer to view the specific as a manifestation of the general, rather than the rule as a surrogate for the example.)

This same style of argument makes the preexisting bias hypothesis more sensible. We need not postulate a preexisting bias for seeing and favoring swords on tails. We only require a general behavioral rule (like intermediate familiarity), that might render the specific result (avoiding incest) as a reasonable manifestation. In fact, Basolo suggests that swords may be preferred by females in swordless species because the implanted weapon makes the male look larger in general, and bigger size is a potent spur to female choice in many regimes of sexual selection. Thus, the general cognitive rule would proclaim: Prefer larger males. The specific solution in this case would be: Extended swords give an impression of larger size with little addition of actual bulk. A thousand other pathways might have satisfied the same broad rule, but
Xiphophorus
evolved a sword. Similarly, the preexisting bias in frogs is a basilar papilla tuned to high frequencies, not an irresistible urge to hear a chuck. Again, this bias might have been exploited in many other ways, but
P. pustulosus
evolved a chuck.

The solution is elegant (and probably even true in these cases—what a rare and lovely combination). Evolution is always a wondrous mixture of the quirky and unpredictable (usually expressed as historical legacies brought to different modern contexts) with the sensible adaptive improvements wrought by natural selection. The quirky component of historical legacy constrains the predictable force of immediate selection, so we usually think of history as restrictive and selection as flexible. But the stories of this essay reverse the usual perspective. Here, historical legacy is a broad cognitive rule bursting with potential along a thousand possible pathways—prefer larger males, or prefer individuals of intermediate familiarity. And adaptation then clamps the limit by choosing one manifestation—a sword, a chuck, or a first cousin. If Lady Luck smiles on the beginning of such an evolutionary trend from one side of our great seal, I am tempted to quote the more familiar motto from the other side to describe the final choice of a singular solution:
E pluribus unum
, one from many.

IN THE OPENING
sentence of
Hereditary Genius
(1869), the founding document of eugenics, Francis Galton (Charles Darwin’s brilliant and eccentric cousin—see Essay 31 for another tale of this remarkable man) proclaimed that “a man’s natural abilities are derived by inheritance.” He then added, making an appeal by analogy to changes induced by domestication:

Darwin had also invoked domestication as his first argument in the
Origin of Species
. Darwin began his great treatise, not with fanfare or general proclamation, but with a discussion of breeding in domestic pigeons (see Essay 25).

Darwin attributed the wondrous variety among pigeons, dogs, and other domesticated animals to the nearly limitless power of selection: “Breeders habitually speak of an animal’s organization as something plastic, which they can model almost as they please.” He quotes one authority on the “great power of this principle of selection”: “It is the magician’s wand, by means of which he may summon into life whatever form and mold he pleases.”

This optimistic notion—that diligence in selection can produce almost any desired trait by artificial selection of domesticated animals or cultivated plants—has inspired the customary extrapolation into nature’s larger scales, leading to a conclusion that natural selection must work even more inexorably to hone wild creatures to a state of optimal design. As Darwin wrote:

This common claim for organic optimality cannot be reconciled with a theme that I regard as the primary message of history—the lesson of the panda’s thumb and the flamingo’s smile: The quirky hold of history lies recorded in oddities and imperfections that reveal pathways of descent. The allure of perfection speaks more to our cultural habits and instructional needs than to nature’s ways (good design inspires wonder and provides excellent material for boxed illustrations in textbooks). Optimality in complex structure would probably bring evolution to a grinding halt, as flexibility disappeared on the altar of intricate adaptation (how might we change a peacock for different environments of its unknown future?).

In any case, leaving aside the abstractions of how nature ought to work, we have abundant empirical evidence that enormous effort in husbandry does not always bring its desired reward. Poultrymen have never broken the “egg-a-day barrier” (no breed of hen consistently lays more than one egg each day), and we are now trying to produce frost-resistant plants by introducing foreign DNA with techniques of genetic engineering because we have not been able to develop such traits by selection upon the natural variation of these plants. We do not know whether such failures represent our own stupidity or lack of sufficient diligence (or time) or whether they record intrinsic structural and genetic limits upon the power of selection. In any case, selection, either natural or artificial, is not the agent of organic optimality that our newspapers and textbooks so often portray. Limits are as powerful and interesting a theme as engineering triumph.

Francis Galton himself, in the same book that promised so much for human futures by controlled breeding, presented our most incisive metaphor for the other side of the coin—the limits to improvement imposed by inherited form and function. (Darwin was also intrigued by the subject of limits and devoted as much attention to this aspect of growth and development as to natural selection itself—see his longest book, the two-volume
Variation in Animals and Plants Under Domestication
, 1868.) Following the optimistic notion of unrestricted molding, we might view an organism as a billiard ball lying on a smooth table. The pool cue of natural selection pushes the ball wherever environmental pressure or human intent dictates. The speed and direction of motion (evolutionary changes) are controlled by the external force of selection. The organism, in short, does not push back. Evolution is a one-way street; outside pushes inside.

But suppose, Galton argues, organisms are not passive spheres but polyhedrons resting upon stable facets.

Galton proposes no new force. The polyhedral stone will not move at all unless natural selection pushes hard. But the polyhedron’s response to selection is restricted by its own internal structure; it can only move to a limited number of definite places. Thus, following the metaphor of Galton’s polyhedron to its conclusion, the actual directions of evolutionary change record a dynamic interaction of external push and internal constraint. The constraints are not merely negative limits to Panglossian possibilities, but active participants in the pathways of evolutionary change. St. George Mivart, whom Darwin acknowledged as his most worthy critic, adopted Galton’s polyhedron as the basis of his argument and wrote (1871):

If Galton’s polyhedron ranks as more than mere verbiage, then we must be able to map the facets of genetic and developmental possibility. We must recast our picture of evolution as an interaction of outside (selection) and inside (constraint), not as an untrammeled trajectory toward greater adaptation. We can find no better subject for investigating facets than Darwin’s own prototype for evolutionary arguments—changes induced in historical time through conscious selection by breeders upon domesticated animals. I can imagine no better object than our proverbial best friend—the dog—Galton’s own choice for comparison in the very first sentence of his manifesto for human improvement.

We should begin by asking why dogs, cows, and pigs, rather than zebras, seals, and hippos are among our domesticated animals? Are all creatures malleable to our tastes and needs, and do our selections therefore reflect the best possible beef and service? Or do some of the strongest and tastiest not enter our orbit because selection cannot overcome inherited features of form or behavior that evolved in other contexts and now resist any recruitment to human purposes?

From the first—or at least since Western traditions abandoned the idea that God had designed creatures explicitly for human use—biologists have recognized that only certain forms of behavior predispose animals to domestication and that our successes represent a subset of available species, not by any means an optimally chosen few amidst unlimited potential. In particular, we have recruited our domestic animals from social species with hierarchies of rank and domination. In the basic “trick” of domestication—what we call “taming” in our vernacular—we learn the animal’s own cues and signals, thus assuming the status of a dominant creature within the animal’s own species. We tame creatures by subverting their own natural behavior. If animals do not manifest a basic sociability and propensity to submit under proper cues, then we have not been able to domesticate them, whatever their potential as food or beast of burden. As Charles Lyell wrote in 1832:

The dog is our primary pet because its ancestor, the wolf
Canis lupus
, had evolved behaviors that, by a fortunate accident of history, included a predisposition for human companionship. Thus, our story begins with a push onto a facet of Galton’s polyhedron. Domestication required a preexisting structure of behavior.

We might readily admit this prerequisite, yet marvel at the stunning diversity of domestic breeds and conclude that any shape or habit might be modeled from the basic wolf prototype. We would be wrong again.

We can usually formulate “big” questions easily enough; the key to good science lies in our ability to translate such ideas into palpable data that can help us to decide one way or the other. We can readily state the issue of limits versus optimality, but how shall we test it? In most cases, we approach such generalities best by isolating a small corner that can be defined and assessed with precision. This tactic often disappoints nonscientists, for they feel that we are being paltry or meanspirited in focusing so narrowly on one particular; yet I would rather tackle a well-defined iota, so long as I might then add further bits on the path to omega, than meet a great issue head-on in such ill-formed complexity that I could only waffle or pontificate about the grand and intangible.

A standard strategy for the study of limits lies in the field of
allometry
, or changes in shape associated with variation in size. Two sequences of size differences might be important for studying variation in form among breeds of domestic dogs:
ontogeny
, or changes in shape that occur during growth of individual dogs from fetus to adult; and
interspecific scaling
, or differences in shape among adults of varying sizes within the family Canidae, from small foxes to large wolves. We might search for regularities in the relationship between size and shape in these two sequences and then ask whether variation among dog breeds follows or transcends these patterns. If, for all their stunning diversity, dogs of different breeds end up with shapes predicted for their size by the ontogenetic or interspecific series, then inherited patterns of growth and history constrain current selection along channels of preferred form. Growth and previous evolution will act as facets of Galton’s polyhedron, favored positions imposed from within upon the efforts of breeders.

The biological literature includes a large but obscure series of articles (mostly
auf Deutsch
), dating to the early years of this century, on allometry in domestic breeds. These themes have been neglected by English and American evolutionists during the past thirty years, primarily because an overconfident, strict Darwinism had so strongly emphasized the power of adaptation that the older subject of limits lost its appeal. But exciting progress in our understanding of genetic architecture and embryological development has begun to strike a proper balance between the external strength of selection and the internal channels of inherited structure. I sense a welcome reappearance of Galton’s polyhedron in the primary technical literature of evolutionary biology. As one example, consider a recent study of ontogenetic and interspecific allometry in dogs by Robert K. Wayne.

Wayne asks how inherited patterns of allometry might constrain the variety of domestic breeds. He finds, for example, that all measures of skull length (face, jaws, and cranium) show little variation in three senses: First, the ontogenetic and interspecific patterns are similar (baby dogs look like small foxes in the portions of length elements); second, we note little change of shape as size increases (baby dogs are like old dogs, and small foxes are like large wolves); third, we find little variation among breeds or species at any common size (all young dogs of the same size have roughly equal length elements).

These three observations suggest that natural variation among canids offers little raw material for fanciers to create breeds with exotic skull lengths. Wayne has confirmed this suspicion by noting that few adults of different breeds, from toy poodle to Great Dane, depart far from the tight relationship predicted by ontogeny or interspecies scaling: The length elements of a small breed may be predicted from the proportions of puppies in larger breeds or from small adult foxes.

Wayne points out that the criteria of artificial selection in domesticated races (the quirky human preferences imposed upon toy or fancy breeds, for example) must differ dramatically from the basis of natural selection in wild species—“the dog’s ability to catch, dismember, or masticate live prey.” If length elements are so constant in such radically different contexts, then their invariance probably reflects an intrinsic limit on variability rather than a fortuitous concurrence in different circumstances. Wayne concludes: